The Annunciation Church in Arzamas, one of the oldest parish churches in the city, was founded in the 17th century and was located near the Spaso-Transfiguration Monastery, on the left side of the ravine that separated the city from the settlement. Until 1775, there were two churches on this site, united in one parish: a wooden, cold church dedicated to the Annunciation of the Most Holy Theotokos, with two chapels, the right in honor of St. John the Baptist and the left in honor of Archangel Michael, and a stone, warm church in honor of the three universal saints, Basil the Great, Gregory the Theologian, and John Chrysostom, also with two chapels, the right in honor of St. Nicholas the Wonderworker and the left in honor of St. Paraskeva Friday. Next to the churches was the parish cemetery.

Construction of the new Annunciation Church began in 1775 and was completed in 1788. The funds for construction were raised by parishioners who sought quality and reliability. The church was two-storied: the first floor was warm, and the second was cold. The church had six altars dedicated to the same saints as in the old churches, and even the antimins remained the same, having served for over a hundred years. The architecture of the church was successfully chosen and partially borrowed from the Assumption Cathedral of the Sarov Monastery. Parishioners actively participated in the construction, with even young girls helping by bringing bricks to the masons.

In 1777, the abbot Joasaph from the Arzamas Spaso-Transfiguration Monastery consecrated all three altars in the lower warm church. In 1784, Bishop Viktor of Vladimir and Murom consecrated the main altar in honor of the Annunciation of the Most Holy Theotokos. The other two chapels were consecrated in 1788 by Archpriest John Andreev.

On April 18, 1928, the city authorities decided to close 11 churches, including the Annunciation Church, to use their buildings for schools and hospitals. Following the decision of the Presidium of the All-Russian Central Executive Committee of the RSFSR on January 25, 1929, it was decided to close 7 parishes, including the Annunciation, where a school was planned to be located. The authorities were interested in the church's wealth: the total weight of the bells was 1214 poods, and 1647 kg of gilded copper was removed from the domes. The gilded iconostasis, candlesticks, and silver vestments of the icons were also confiscated.

In the 1930s, the church, stripped of its domes, was used as a dormitory for students of the pedagogical college. In the last years of Soviet power, the first floor housed a workshop for producing monuments, while the second floor was the office of the trust for canteens and restaurants.

In 2004, the building was transferred to the Church and assigned to the restoring Spaso-Transfiguration Monastery, and repair work began. The first service was held on Christmas in 2006. Now, regular monastic services are conducted in the church.